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The Puzzling Falcomurus Mandal (Collembola, Orchesellidae, Heteromurinae): a Review

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The Puzzling Falcomurus Mandal (Collembola, Orchesellidae, Heteromurinae): a Review insects Article The Puzzling Falcomurus Mandal (Collembola, Orchesellidae, Heteromurinae): A Review Bruno C. Bellini 1,* , Paolla G. C. de Souza 1 and Penelope Greenslade 2,3,* 1 Laboratório de Collembola, Departamento de Botânica e Zoologia, Centro de Biociências, Campus Universitário, Universidade Federal do Rio Grande do Norte—UFRN. BR 101, Lagoa Nova, Natal 59072-970, Brazil; [email protected] 2 School of Science, Psychology and Sports, Federation University, Ballarat, VIC 3353, Australia 3 Department of Biology, Australian National University, GPO Box, Canberra, ACT 0200, Australia * Correspondence: [email protected] (B.C.B.); [email protected] (P.G.) Simple Summary: Springtails are tiny microarthropods found mainly in soil habitats around the globe. Falcomurus is a genus of Heteromurinae (Orchesellidae), currently with a single species from India. Here, we revise the genus, transferring Dicranocentrus litoreus Mari-Mutt and D. halophilus Mari-Mutt to Falcomurus and describing two new taxa from marine littoral habitats in Australian archipelagos. We discovered the morphology of Falcomurus is quite similar among its species, but some characters of its chaetotaxy (the distribution and morphology of body chaetae) are useful to clearly separate them from each other. Abstract: Falcomurus Mandal is currently a monotypic genus of Heteromurinae described from India in 2018. Its key characters are the first antennal segment subdivided, the second undivided and the third annulated; the first abdominal segment lacking macrochaetae; and the presence of a sinuous modified macrochaeta on the proximal dens. Some details of its morphology were recently put in doubt, and so its genus status and affinities remain uncertain. Here, we revise Citation: Bellini, B.C.; Souza, P.G.C.d.; Greenslade, P. The Puzzling the genus based on the type material of Dicranocentrus litoreus Mari-Mutt, as well as provide the Falcomurus Mandal (Collembola, description of two new species from Australian archipelagos and a reinterpretation of the chaetotaxy Orchesellidae, Heteromurinae): A of Falcomurus chilikaensis Mandal and D. halophilus Mari-Mutt. After our revision, Falcomurus shows a Review. Insects 2021, 12, 650. https:// well-conserved chaetotaxy and overall morphology, which allowed us to provide an updated generic doi.org/10.3390/insects12070650 diagnosis. While the antennae morphology of Falcomurus resembles that of Dicranocentrus Schött, its dorsal sensillar and macrochaetotaxy suggest it is closely related to Heteromurus Wankel, as originally Academic Editor: Stewart B. Peck stated by Mandal. The main features useful to separate Falcomurus species are the head, mesothorax and fourth abdominal segment chaetotaxy. We also provide a key to its five species, a comparative Received: 1 June 2021 table and notes on the affinities and distribution of Falcomurus. Accepted: 24 June 2021 Published: 16 July 2021 Keywords: chaetotaxy; Entomobryoidea; Entomobryomorpha; Heteromurini; taxonomy Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affil- 1. Introduction iations. Recent studies reviewing the systematics within the Entomobryoidea have improved the understanding of the relationships between the families, subfamilies, tribes and genera, plus identified new more reliable diagnostic characters [1–3]. In particular, the affinities and internal organisation of the Orchesellinae sensu Soto-Adames et al. [4] were revised, Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. and this taxon was reinstated as a full family, as earlier proposed [3,5]. Other studies This article is an open access article have provided more evidence to support the validity and possible relationships within distributed under the terms and the Orchesellidae and suggested the sensillar pattern of the trunk segments may better conditions of the Creative Commons distinguish its lineages [3,6–8]. Attribution (CC BY) license (https:// Among the Orchesellidae, the Heteromurinae are defined by the presence of coarsely creativecommons.org/licenses/by/ ciliate scales on the body and a sensillar formula from the dorsal mesothorax to the 4.0/). third abdominal segment of 2,2|1,3,3 [3]. The most recent revisions dealing with the Insects 2021, 12, 650. https://doi.org/10.3390/insects12070650 https://www.mdpi.com/journal/insects Insects 2021, 12, 650 2 of 31 Heteromurinae subdivided it into two tribes and seven genera: Mastigoceras Handschin, 1924 [9] (the sole genus in Mastigocerini); and Alloscopus Börner, 1906 [10], Dicranocentrus Schött, 1893 [11], Heteromurtrella Mari-Mutt, 1979 [12], Heteromurus Wankel, 1860 [13], Pseudodicranocentrus Mari-Mutt, 1981 [14] and Sinodicranocentrus Zhang, 2020 [8] (all from Heteromurini) [1,3,8]. In [8], the status of the recently described Falcomurus Mandal, 2018 [15] in the Heteromurini was disregarded, because of mistakes in its description and similarities with other taxa. Falcomurus is currently a monotypic genus of Heteromurini from India, with many similarities to Heteromurus. Its most striking character is the presence of a sinuous ciliate macrochaeta on the proximal dens [15]. The original description of its dorsal chaetotaxy does not have a clear match among the Heteromurini, with the exception of an absence of macrochaetae on the first abdominal segment, recorded only for Heteromurus, including its subgenus Verhoeffiela Absolon, 1900 [16], and two species of Dicranocentrus, D. litoreus Mari-Mutt, 1985 and D. halophilus Mari-Mutt, 1985 [8,15,17]. These Dicranocentrus species actually show more similarities with Heteromurus concerning their dorsal chaetotaxy and also present the same sinuous dental macrochaeta described in Falcomurus [17] (p. 313, Figure 69 and pp. 318–320). Unlike the Northern Hemisphere collembolan faunas, the Orchesellidae fauna of Australia is represented by few species in few genera, all with limited distributions. There is only one species of Heteromurus, H. major (Moniez, 1889) [18], introduced and only found in very disturbed habitats, such as home gardens or public parks. The common, abundant and widespread genus Orchesella Templeton, 1836 [19] of the Northern Hemisphere, is not present. The genera that are present are Alloscopus, Australotomurus Stach, 1947 [20] and Isotobrya Womersley, 1934 [21], with one, seven and two species, respectively [22]. The species in each of the genera live in different habitats, such as soil, coastal and montane heathland and termite nests, respectively. Both Australotomurus and Isotobrya are endemic to Australia and it appears they are representatives of a more ancient, now relict, fauna than the present dominant genus of Entomobryoidea, Entomobrya Rondani, 1861 [23]. Here, we provide a review of Falcomurus based on the literature, a revision of the Dicranocentrus litoreus type material and the description of two new Australian species from tropical marine littoral habitats. Using a comparative morphological analysis, we reinterpreted the dorsal chaetotaxy and other morphological features of its type species. A revised generic diagnosis, discussion on the generic affinities, key to its species and a comparative table of their main features are also presented. 2. Materials and Methods Specimens of the new species were mounted on glass slides in Berlese’s medium. Morphological studies and raw drawings were made with a Leica DM750 microscope with an attached drawing tube. Photographs were taken with a Leica MC170 HD camera attached to the microscope, using LAS 4.12 software. The final figures were digitized and organized in plates using CorelDraw X8 software. The type series is deposited at the Museum of Victoria, Melbourne, Australia, under the acronym of MVMA. The chaetotaxy terminology used in this study mainly follows Fjellberg [24] for labial palp papillae; Gisin [25] for labial chaetotaxy, with additions of Zhang and Pan [26] and using Bellini et al. [27] as a model; Cipola et al. [28] for labral chaetotaxy; Mari-Mutt [29] for dorsal head chaetotaxy, with additions of Soto-Adames [30] and Zhang et al. [8]; Szeptycki [31] and Zhang and Deharveng [1] for S-chaetotaxy; and Szeptycki [32] for dorsal chaetotaxy, with additions and modifications provided by Soto-Adames [30], Cipola et al. [33] and Zhang et al. [3,8,34], using also Bellini et al. [27] as a model. The abbreviations used in the descriptions are Abd.—abdominal segment(s); Ant.— antennal segment(s); mac—macrochaeta(e); mes—mesochaeta(e); mic—microchaeta(e); ms—S-microchaeta(e); sens—ordinary S-chaeta(e); and Th.—thoracic segment(s). Antennal segments I and II’s subdivisions are ‘a’ for the proximal subarticle and ‘b’ for the distal one. Insects 2021, 12, 650 3 of 31 The symbols used in the drawings to represent the dorsal chaetotaxy patterns are large blank circles for mac; large black circles for mes; small black circles for mic; blank circles with a small black circle inside for mac or mic; black chaetae-like drawings for sens or ms; black circles crossed by a line for pseudopores; ciliate chaetae-like symbols for bothriotricha; and a dash above or under any symbol for chaetae presence or absence. Taxonomic descriptions and comparisons were based on a half body. Chaetae labels (including rows/series) and labial papillae are marked in bold throughout the text. 3. Results 3.1. Taxonomic Summary and Genus Diagnosis • Order Entomobryomorpha Börner, 1913 [35] • Superfamily Entomobryoidea Womersley, 1934 [21] • Family Orchesellidae Börner, 1906 [10], sensu
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